Infants' dietary arsenic exposure during transition to solid food

Antonio J Signes-Pastor, Kathryn L Cottingham, Manus Carey, Vicki Sayarath, Thomas Palys, Andrew A Meharg, Carol L Folt, Margaret R Karagas, Antonio J Signes-Pastor, Kathryn L Cottingham, Manus Carey, Vicki Sayarath, Thomas Palys, Andrew A Meharg, Carol L Folt, Margaret R Karagas

Abstract

Early-life exposure to inorganic arsenic (i-As) may cause long-lasting health effects, but as yet, little is known about exposure among weaning infants. We assessed exposure before and during weaning and investigated the association between solid food intake and infants' urinary arsenic species concentrations. Following the recording of a comprehensive 3 day food diary, paired urine samples (pre- and post-weaning) were collected and analyzed for arsenic speciation from 15 infants participating in the New Hampshire Birth Cohort Study. Infants had higher urinary i-As (p-value = 0.04), monomethylarsonic acid (MMA) (p-value = 0.002), dimethylarsinic acid (DMA) (p-value = 0.01), and sum of arsenic species (i-As + MMA + DMA, p-value = 0.01) during weaning than while exclusively fed on a liquid diet (i.e., breast milk, formula, or a mixture of both). Among weaning infants, increased sum of urinary arsenic species was pairwise-associated with intake of rice cereal (Spearman's ρ = 0.90, p-value = 0.03), fruit (ρ = 0.70, p-value = 0.03), and vegetables (ρ = 0.86, p-value = 0.01). Our observed increases in urinary arsenic concentrations likely indicate increased exposure to i-As during the transition to solid foods, suggests the need to minimize exposure during this critical period of development.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Concentrations of urinary arsenic species before (at 4 months of age) and during weaning (at 6 months of age) to solid foods. At 6 months of age infants’ diets included solid food in addition to breast milk, formula, or a mixture of both breast milk and formula. Each infant is identified by a unique color to facilitate the comparison between the two time points. The p-values were derived from paired Wilcoxon signed-rank test analyses. Urinary arsenic species concentrations were natural logarithm transformed to help visualization.
Figure 2
Figure 2
Concentrations of infant urinary arsenic species in relation to intake of specific foods at 6 months of age. Each infant is identified by a unique color. Spearman’s correlation coefficient and p-value for each dietary item. Urinary arsenic species concentration and solid food consumption were natural logarithm transformed to help visualization. The least-squares regression line is also included to help visualize associations. *Infant P14 was not included in Spearman’s correlation between urinary arsenic species content and the formula powder intake level (outlier).

References

    1. EFSA. European Food Safety Authority. Scientific opinion on arsenic in food. EFSA panel on contaminants in food chain (CONTAM). 7 (2009).
    1. Taylor, V. et al. Human exposure to organic arsenic species from seafood. Sci. Total Environ, 10.1016/j.scitotenv.2016.12.113 (2016).
    1. WHO. Environmental Health Criteria 224 ARSENIC AND ARSENIC COMPUNDS (Second Edition). World Heal. Organ. Geneva 1–66 at, (2001).
    1. Cubadda F, et al. Human exposure to dietary inorganic arsenic and other arsenic species: State of knowledge, gaps and uncertainties. Sci. Total Environ. 2016;579:1228–1239. doi: 10.1016/j.scitotenv.2016.11.108.
    1. Molin M, Ulven SM, Meltzer HM, Alexander J. Arsenic in the human food chain, biotransformation and toxicology – Review focusing on seafood arsenic. J. Trace Elem. Med. Biol. 2015;31:249–259. doi: 10.1016/j.jtemb.2015.01.010.
    1. Jansen RJ, et al. Determinants and consequences of arsenic metabolism efficiency among 4,794 individuals: Demographics, lifestyle, genetics, and toxicity. Cancer Epidemiol. Biomarkers Prev. 2016;25:381–390. doi: 10.1158/1055-9965.EPI-15-0718.
    1. Tseng CH. A review on environmental factors regulating arsenic methylation in humans. Toxicol. Appl. Pharmacol. 2009;235:338–350. doi: 10.1016/j.taap.2008.12.016.
    1. Antonelli R, Shao K, Thomas DJ, Sams R, Cowden J. AS3MT, GSTO, and PNP polymorphisms: Impact on arsenic methylation and implications for disease susceptibility. Environ. Res. 2014;132:156–167. doi: 10.1016/j.envres.2014.03.012.
    1. Orloff K, Mistry K, Metcalf S. Biomonitoring for environmental exposures to arsenic. J. Toxicol. Environ. Health. B. Crit. Rev. 2009;12:509–524. doi: 10.1080/10937400903358934.
    1. Molin M, et al. Humans seem to produce arsenobetaine and dimethylarsinate after a bolus dose of seafood. Environ. Res. 2012;112:28–39. doi: 10.1016/j.envres.2011.11.007.
    1. Signes-Pastor AJ, et al. Concentrations of urinary arsenic species in relation to rice and seafood consumption among children living in Spain. Environ. Res. 2017;159:69–75. doi: 10.1016/j.envres.2017.07.046.
    1. IARC. A., Metals, Fibers. & Dusts. A review of human carcinogens. IARC monographs on the evaluation of carcinogenic risks to humans. 100C, 527 (2012).
    1. Sanchez TR, Perzanowski M, Graziano JH. Inorganic arsenic and respiratory health, from early life exposure to sex-specific effects: A systematic review. Environ. Res. 2016;147:537–555. doi: 10.1016/j.envres.2016.02.009.
    1. Nachman KE, et al. Mitigating dietary arsenic exposure: Current status in the United States and recommendations for an improved path forward. Sci. Total Environ. 2017;581–582:221–236. doi: 10.1016/j.scitotenv.2016.12.112.
    1. Signes-Pastor AJJ, et al. Levels of infants’ urinary arsenic metabolites related to formula feeding and weaning with rice products exceeding the EU inorganic arsenic standard. Plos One. 2017;12:e0176923. doi: 10.1371/journal.pone.0176923.
    1. Karagas MR, et al. Association of Rice and Rice-Product Consumption With Arsenic Exposure Early in Life. JAMA Pediatr. 2016;3766:1–8.
    1. Kurzius-Spencer M, et al. Contribution of diet to aggregate arsenic exposures-an analysis across populations. J. Expo. Sci. Environ. Epidemiol. 2014;24:156–62. doi: 10.1038/jes.2013.37.
    1. Farzan SF, et al. In utero arsenic exposure and infant infection in a United States cohort: A prospective study. Environ. Res. 2013;126:24–30. doi: 10.1016/j.envres.2013.05.001.
    1. Feldmann J, Krupp EM. Critical review or scientific opinion paper: Arsenosugars-a class of benign arsenic species or justification for developing partly speciated arsenic fractionation in foodstuffs? Anal. Bioanal. Chem. 2011;399:1735–1741. doi: 10.1007/s00216-010-4303-6.
    1. Fängström B, et al. Breast-feeding protects against arsenic exposure in Bangladeshi infants. Environ. Health Perspect. 2008;116:963–969. doi: 10.1289/ehp.11094.
    1. Vahter M. Effects of Arsenic on Maternal and Fetal Health. Annu. Rev. Nutr. 2009;29:381–399. doi: 10.1146/annurev-nutr-080508-141102.
    1. Carignan, C. C., Cottingham, K. L., Jackson, B. P., Farzan, S. F. & Gandolfi, A. J. Estimated Exposure to Arsenic in Breastfed and Formula-Fed Infants in a United States Cohort. 500, 500–507 (2015).
    1. WHO WHO guidelines for drinking-water quality. WHO Chron. 2011;38:104–108.
    1. EPA, U. S. Drinking Water Standard for Arsenic at, (2001).
    1. Jackson BP, Taylor VF, Punshon T, Cottingham KL. Arsenic concentration and speciation in infant formulas and first foods. Pure Appl. Chem. 2012;84:215–223. doi: 10.1351/PAC-CON-11-09-17.
    1. Carignan CC, Karagas MR, Punshon T, Gilbert-Diamond D, Cottingham KL. Contribution of breast milk and formula to arsenic exposure during the first year of life in a US prospective cohort. J. Expo. Sci. Environ. Epidemiol. 2016;26:452–457. doi: 10.1038/jes.2015.69.
    1. Williams PN, et al. Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ. Sci. Technol. 2007;41:6854–6859. doi: 10.1021/es070627i.
    1. Signes-Pastor AJ, Carey M, Meharg AA. Inorganic arsenic in rice-based products for infants and young children. Food Chem. 2016;191:128–134. doi: 10.1016/j.foodchem.2014.11.078.
    1. Carbonell-Barrachina AA, et al. Inorganic arsenic contents in rice-based infant foods from Spain, UK, China and USA. Environ. Pollut. 2012;163:77–83. doi: 10.1016/j.envpol.2011.12.036.
    1. Lynch HN, Greenberg GI, Pollock MC, Lewis AS. A comprehensive evaluation of inorganic arsenic in food and considerations for dietary intake analyses. Sci. Total Environ. 2014;496:299–313. doi: 10.1016/j.scitotenv.2014.07.032.
    1. Hinwood AL, et al. Are 24-hour urine samples and creatinine adjustment required for analysis of inorganic arsenic in urine in population studies? Environ. Res. 2002;88:219–24. doi: 10.1006/enrs.2002.4339.
    1. Meharg AA, et al. Urinary excretion of arsenic following rice consumption. Environ. Pollut. 2014;194:181–7. doi: 10.1016/j.envpol.2014.07.031.
    1. Nermell B, et al. Urinary arsenic concentration adjustment factors and malnutrition. Environ. Res. 2008;106:212–218. doi: 10.1016/j.envres.2007.08.005.
    1. Nestlé Pure Life Nestlé Waters. Bottled Water Quality Report. 1–22, at, (2012).
    1. WHO. Infant and young child feeding Model Chapter for textbooks for medical students and allied health professionals at, (2009).
    1. Ljung K, Palm B, Grandér M, Vahter M. High concentrations of essential and toxic elements in infant formula and infant foods - A matter of concern. Food Chem. 2011;127:943–951. doi: 10.1016/j.foodchem.2011.01.062.
    1. Brown RM, Newton D, Pickford CJ, Sherlock JC. Human Metabolism of Arsenobetaine. Hum. Exp. Toxicol. 1990;9:41–46. doi: 10.1177/096032719000900109.
    1. Stiboller M, Raber G, Gjengedal ELF, Eggesbø M, Francesconi KA. Quantifying Inorganic Arsenic and Other Water-Soluble Arsenic Species in Human Milk by HPLC/ICPMS. Anal. Chem. 2017;89:6265–6271. doi: 10.1021/acs.analchem.7b01276.
    1. FDA. FDA proposes limit for inorganic arsenic in infant rice cereal at, (2016).
    1. EC. Commission Regulation 2015/1006 of 25 June 2015 amending Regulation (EC) No 1881/2006 as regards maximum levels of inorganic arsenic in foodstuffs, doi:eur-lex.474 (2015).
    1. Signes-Pastor AJJ, et al. Geographical variation in inorganic arsenic in paddy field samples and commercial rice from the Iberian Peninsula. Food Chem. 2016;202:356–363. doi: 10.1016/j.foodchem.2016.01.117.
    1. Meharg AA, et al. Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ. Sci. Technol. 2009;43:1612–7. doi: 10.1021/es802612a.
    1. Kordas K, et al. Low-level arsenic exposure: Nutritional and dietary predictors in first-grade Uruguayan children. Environ. Res. 2016;147:16–23. doi: 10.1016/j.envres.2016.01.022.
    1. FDA. Search for FDA Guidance Documents - Draft Guidance for Industry: Arsenic in Apple Juice - Action Level. at, (2013).
    1. NFHPC. China’s Maximum Levels for Contaminants in Foods China -Peoples Republic of National Food Safety Standard for Maximum Levels of Contaminants in Foods. At, GAIN Publications/Maximum Levels of Contaminants in Foods _Beijing_China - Peoples Republic of_12-11-2014.pdf (2012).
    1. EC. Arsenic in food. At, (2017).
    1. Tao SS, Bolger PM. Dietary arsenic intakes in the United States: FDA Total Diet Study, September 1991-December 1996. Food Addit. Contam. 1999;16:465–472. doi: 10.1080/026520399283759.
    1. Signes-Pastor AJ, et al. Arsenic Speciation in Food and Estimation of the Dietary Intake of Inorganic Arsenic in a Rural Village of West Bengal, India. J. Agric. Food Chem. 2008;56:9469–9474. doi: 10.1021/jf801600j.
    1. Carbonell-Barrachina AA, Signes-Pastor AJ, Vázquez-Araújo L, Burló F, Sengupta B. Presence of arsenic in agricultural products from arsenic-endemic areas and strategies to reduce arsenic intake in rural villages. Mol. Nutr. Food Res. 2009;53:531–541. doi: 10.1002/mnfr.200900038.
    1. Punshon T, et al. Understanding arsenic dynamics in agronomic systems to predict and prevent uptake by crop plants. Sci. Total Environ. 2017;581–582:209–220. doi: 10.1016/j.scitotenv.2016.12.111.
    1. Gilbert-Diamond D, et al. Rice consumption contributes to arsenic exposure in US women. Proc. Natl. Acad. Sci. USA. 2011;108:20656–60. doi: 10.1073/pnas.1109127108.
    1. Signes-Pastor AJJ, et al. Urinary Arsenic Speciation in Children and Pregnant Women from Spain. Expo. Heal. 2017;9:105–111. doi: 10.1007/s12403-016-0225-7.
    1. R Core Team. R: A Language and Enrionment for Statistical Computing, R Foundation for Statisical Computing, doi: (2014).

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